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Ptolemeba N. Gen., a Novel Genus of Hartmannellid Amoebae (Tubulinea, Amoebozoa); with an Emphasis on the Taxonomy of Saccamoeba

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Ptolemeba N. Gen., a Novel Genus of Hartmannellid Amoebae (Tubulinea, Amoebozoa); with an Emphasis on the Taxonomy of Saccamoeba The Journal of Published by the International Society of Eukaryotic Microbiology Protistologists Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Ptolemeba n. gen., a Novel Genus of Hartmannellid Amoebae (Tubulinea, Amoebozoa); with an Emphasis on the Taxonomy of Saccamoeba Pamela M. Watsona, Stephanie C. Sorrella & Matthew W. Browna,b a Department of Biological Sciences, Mississippi State University, Mississippi State, Mississippi, 39762 b Institute for Genomics, Biocomputing & Biotechnology, Mississippi State University, Mississippi State, Mississippi, 39762 Keywords ABSTRACT 18S rRNA; amoeba; amoeboid; Cashia; cristae; freshwater amoebae; Hartmannella; Hartmannellid amoebae are an unnatural assemblage of amoeboid organisms mitochondrial morphology; SSU rDNA; SSU that are morphologically difficult to discern from one another. In molecular phy- rRNA; terrestrial amoebae; tubulinid. logenetic trees of the nuclear-encoded small subunit rDNA, they occupy at least five lineages within Tubulinea, a well-supported clade in Amoebozoa. The Correspondence polyphyletic nature of the hartmannellids has led to many taxonomic problems, M.W. Brown, Department of Biological in particular paraphyletic genera. Recent taxonomic revisions have alleviated Sciences, Mississippi State University, some of the problems. However, the genus Saccamoeba is paraphyletic and is Mississippi State, MS 39762, USA still in need of revision as it currently occupies two distinct lineages. Here, we Telephone number: +1 662-325-2406; report a new clade on the tree of Tubulinea, which we infer represents a novel FAX number: +1 662-325-7939; genus that we name Ptolemeba n. gen. This genus subsumes a clade of hart- e-mail: [email protected] mannellid amoebae that were previously considered in the genus Saccamoeba, but whose mitochondrial morphology is distinct from Saccamoeba. In accor- Received: 6 March 2014; revised 7 May dance with previous research, we formalize the clade as distinct from Sacc- 2014; accepted May 8, 2014. amoeba. Transmission electron microscopy of our isolates illustrate that both molecularly discrete species can be further differentiated by their unique mito- doi:10.1111/jeu.12139 chondrial cristal morphology. HARTMANNELLIDAE Volkonsky, 1931 is a family of limax- Dykova et al. 2008). The hartmannellids have recently shaped amoebae within Tubulinea of Amoebozoa (Adl been reviewed and redefined (Brown et al. 2011; Smirnov et al. 2012). The family classically includes the genera et al. 2011). Hartmannella, Cashia, Glaeseria, and Saccamoeba (Page The two most speciose hartmannellid genera are Hart- 1974, 1988). These genera are morphologically difficult to mannella and Saccamoeba; however, both genera appear ascertain between taxa, and recent molecular data have to be paraphyletic in molecular phylogenetic reconstruc- proven that the lines between the genera are particularly tions (Dykova et al. 2008). The fundamental difference skewed. The most challenging aspect is that hartmannel- between the two genera is that Saccamoeba lacks a lids look very similar to one another in terms of gross mor- distinctive hyaline cap on its monotactic pseudopodium, phology. Generally, the trophozoites are elongate with a unlike the distinctive hyaline cap observed in Hartmannella high length to breadth of ratio, typically > 4 (Page 1988). (Page 1988). Hartmannella has been recently redefined They most often move in a monotactic fashion, with non- according to molecular phylogenetics in Brown et al. monotactic pseudopodial extensions resulting in abrupt (2011) and is beginning to be taxonomically resolved changes in direction that can be somewhat eruptive in (Smirnov et al. 2011). However, Saccamoeba is still fashion. Cells are uninucleate with a vesicular nucleolus. greatly in need of revision. The first molecular assignation In addition, molecular phylogenetic trees have shown that of Saccamoeba was in 2000 from an isolate earlier identi- even though the hartmannellids are superficially alike at fied at the American Type Culture Collection (ATCC) as the morphological level they are polyphyletic, comprising Saccamoeba limax (ATCC 30942) (Amaral Zettler et al. at least four different clades in nuclear-encoded small 2000). Dykova et al. (2002)isolated an amoeba (strain subunit rDNA (SSU rDNA) trees (Brown et al. 2011; LOS7N) that is nearly identical in SSU rDNA sequence © 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists Journal of Eukaryotic Microbiology 2014, 0, 1–9 1 Ptolemeba n. gen., a New Hartmannellid Genus Watson et al. (99.58% uncorrected pairwise distance [upd]) to ATCC 0.75 g K2HPO4, 15.0 g agar, and 1 liter ddH2O) Petri 30942, S. limax sensu (Amaral Zettler et al. 2000). They plates. The plates were then incubated for 4 d and examined strain LOS7N under transmission electron observed with a 10X objective under a compound micro- microscopy (TEM) and found that it has unique tubular scope. On the edges of the absorbed water droplet amoe- mitochondrial cristae that are arranged in an unusual heli- bae were observed. For all strains, a single amoeba cell cal pattern that is very uniform (Dykova et al. 2002). This was isolated using a flame sterilized 30-gage platinum cristal configuration is clearly dissimilar to previous TEM wire micro loop, where the loop was used to drag a single reports of S. limax sensu Page, 1985; which has branching amoeba along the agar surface to isolate it away from all tubular cristae that do not appear to have a uniform other eukaryotes on the inoculated plate. Each culture arrangement (Page 1985). Later, Dykova et al. (2008) iso- was established as clonal with no other accompanying lated a new strain (NTSHR) assigned to Saccamoeba that eukaryotes. Cultures are maintained through monthly pas- appears to be very similar to Page’s concept of S. limax in sage onto fresh wMY plates inoculated with a streak of both light and TEM morphology. However, strain NTSHR Escherichia coli (strain K-12 MG1655) as a food source. branches distantly away from S. limax sensu Amaral Zet- Cultures Nx13-1a and SK13-4e have been deposited with tler et al. 2000 (Dykova et al. 2008). This led Dykova et al. the ATCC under accession PRA-414 and PRA-415, respec- to recognize NTSHR as a representative strain of Sacc- tively. amoeba and that S. limax sensu Amaral Zettler et al. (2000) should be considered a distinct genus. However, Light microscopy they did not propose a name for that clade of strains. Although helical patterning of mitochondrial cristae is All light micrographs were taken using a Zeiss AxioSkop 2 observed in the morphologically similar genus Cashia (Carl Zeiss Microimaging, Thornwood, NY) connected to (Page, 1985) as noted by Dykova et al. 2008; the pattern- an 18-megapixel Canon 650D color digital camera (Canon, ing of Cashia is much less pronounced and less uniform Melville, NY). Image capture was performed by use of than in NTSHR (compare fig. 1E–H of Dykova et al. 2008 Canon’s image capture software (EOS Utility; Canon). to fig. 27 and 28 of Page 1985). Observations and photomicrographs using differential Here, we present three novel isolates of freshwater/soil interference contrast optics were made by inoculating a amoebae that were obtained from samples collected from drop of wMY liquid media with amoebae taken from agar eastern-central Mississippi. Our isolates have a general plates onto glass slides covered with a coverslip. Mea- appearance of saccamoebids, with limax-type morphology surements were taken using the measurement function of and frequently lack a distinctive hyaline cap. We present ImageJ (Schneider et al. 2012). morphological and ultrastructural data as well as an SSU rDNA phylogeny. One of our strains branches with the DNA extraction taxon “Saccamoeba limax” sensu Amaral Zettler et al. 2000 and LOS7N. Our other two strains are virtually identi- For DNA isolation, Nx13-1a, Nx13-1c, and Sk13-4e were cal to one another at the SSU rDNA level except for a cultured with E. coli (strain K-12 MG1655) on wMY agar 497-bp group I intron in strain Nx13-1c; together they plates at room temperature (ca. 21 °C). DNA was branch as sister to the amoebae with helical cristae, i.e. extracted from two plates of dense growth amoebae ATCC 30942 and LOS7N. using a modified salt extraction method (Aljanabi and Mar- tinez 1997) for use as a template in polymerase chain reaction (PCR) amplifications. Briefly, cells were resus- MATERIALS AND METHODS pended in 5-ml liquid wMY and collected in a 15-ml coni- cal tube. The cells were pelleted by centrifugation at Isolation and culturing 3184 g for 2 min, and the cell pellet was suspended in Strains Nx13-1a and Nx13-1c were isolated from a water 200 ll of salt homogenizing buffer (0.4 M NaCl, 10 mM sample that was collected from Sam D. Hamilton Noxu- Tris–HCl pH 8.0 and 2 mM ethylenediaminetetraacetic bee National Wildlife Refuge (33.273220°N, 88.790542°W) acid [EDTA] pH 8.0). Then proteinase K (20 mg/ml) was on September 2, 2013. The water sample was from water added to the solution to a final concentration of 400 lg/ml that was about 20-cm deep, with a mud sediment bottom. and sodium dodecyl sulfate was added to final concentra- Sediment was also obtained during the water collection. tion of 2%. The sample was mixed by gentle inverting Strain Sk13-4e was isolated from a soil sample that was and then incubated at 56 °C for 1 h. The sample was incu- collected in between the annex and lecture hall of Harned bated on ice for 5 min followed by the addition of one vol- Hall on the Mississippi State University campus, Missis- ume of 5M NaCl [2.5 M]. The sample was then vortexed sippi State, MS, USA (33.455790°N, 88.788123°W) on lightly and spun 14,000 g at 4 °C for 30 min. The superna- September 20, 2013. For the soil sample, as mud slurry tant was moved to a fresh tube and centrifuged again to was made with ~5 g of soil mixed with 15 ml of sterile pellet residual precipitant (14,000 g at 4 °C for 10 min).
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